Distribution of Grape Berry Moth, Endopiza viteana (Lepidoptera: Tortricidae), in Natural and Cultivated Habitats

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1 BEHAVIOR Distribution of Grape Berry Moth, Endopiza viteana (Lepidoptera: Tortricidae), in Natural and Cultivated Habitats NATALIA BOTERO-GARCÉS AND RUFUS ISAACS 1 Department of Entomology, 202 Center for Integrated Plant Systems, Michigan State University, East Lansing, MI Environ. Entomol. 32(5): 1187Ð1195 (2003) ABSTRACT The relative abundance of male grape berry moths, Endopiza viteana Clemens (Lepidoptera: Tortricidae), was studied within Michigan grape agroecosystems during 1999Ð2001. Distribution within and between habitats was determined using pheromone traps placed at different heights between the interior of deciduous woods and interior of adjacent vineyards. Comparisons of relative moth abundance across habitats using traps at the standard 1.5 m sampling height conþrmed that moths are more abundant in the woods in spring and in the vineyard later in the season. Traps placed at 1.5, 3.0, 6.0, and 9.0 m above ground level in woods and vineyards revealed that moth relative abundance increases with height in woods, whereas 90.0% of moths caught in vineyards were at 1.5 m above ground level. Sampling inside the woods up to 15.2 m revealed that 76.1% of moths were found at or above 9.0 m. Relatively few moths were trapped in the interface between these habitats, where grapevines are not present. The results of vertical sampling suggests that moths are not moving from woods to vineyards, but instead are most abundant high in the woods canopy. These results show that the relative abundance of grape berry moth varies within and between habitats, and suggest that distribution of this specialist insect is associated with the distribution of its wild and cultivated host. RÉSUMÉ LÕabondance relative des mâles de la tordeuse de la vigne, Endopiza viteana Clemens (Lepidoptera: Tortricidae), a été étudiée dans lõécosystème agronomique des vignobles du Michigan aux États Unis, durant 1999Ð2001. La distribution relative intra- et inter-habitats (les bois adjacents et les vignobles) a été déterminée par lõutilization de pièges à phéromone placés àdifférentes hauteurs entre lõintérieur des bois et lõintérieur des vignobles contigus. Les comparaisons sur lõabondance relative de mâles en utilisant des pièges placés àla hauteur standard de 1.5 m, ont conþrmé que les mâles sont plus abondants dans les bois au printemps et dans les vignobles plus tard dans la saison. Des pièges placésàdes hauteurs de 1.5, 3.0, 6.0, et 9.0 m dans les bois et les vignobles adjacents ont montré que dans les bois, lõabondance relative augmente à mesure que la hauteur du piège augmente, pendant que dans les vignobles, le 90.0% des mâles capturés se trouvent à la hauteur de 1.5 m par-dessus le sol. En ayant des pièges placés jusquõà une hauteur de 15.2 m dedans les bois, nous avons trouvé que le 76.1% des mâles se trouvaient à ou par-dessus le niveau de neuf mètres. Relativement peu de mâles furent capturés àlõinterface entre ces deux habitats où les vignes sont absentes. Les résultats dõun échantillonnage vertical suggèrent que les mâles ne se déplacent pas des bois vers les vignobles, sinon quõils continuent tout le temps à être plus nombreux dans le haut des bois, les coupes des arbres. LÕabondance relative de la tordeuse de la vigne varie non seulement intra- mais aussi inter-habitats, ce qui suggère que la distribution de cet insecte spécialiste soit associée avecla distribution de son hôte sauvage et cultivé. KEY WORDS Endopiza viteana, Vitis, grape berry moth, ecology, distribution THE GRAPE BERRY MOTH, Endopiza viteana Clemens (Lepidoptera: Tortricidae), is a specialist herbivore, found in vineyards and woods throughout the Eastern United States and Southeastern Canada (Johnson and Hammar 1912). Females lay eggs individually on grape berries and the larvae hatch and enter the berries to feed and develop. When larvae are ready to pupate, they leave the berry for a nearby leaf in which they cut 1 isaacsr@msu.edu. a crescent-shaped section and wrap it around while spinning a cocoon (Slingerland 1904, Johnson and Hammar 1912). First emergence of grape berry moth adults in spring generally occurs during bloom and can vary from early May (Dozier et al. 1932) to early June (Johnson and Hammar 1912, Ingerson 1920, Pettit 1932). Depending on weather conditions, there may be two or more generations per year with widely varying phenologies (Hoffman et al. 1992, Tobin et al. 2002), the last of which overwinters as pupae on X/03/1187Ð1195$04.00/ Entomological Society of America

2 1188 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 5 leaves. When these leaves drop to the ground, the pupae may be blown by the wind to the edges of the vineyard and into woods (Johnson and Hammar 1912). The native ancestral host plant of E. viteana is the wild grape (Vitis spp., Vitaceae) commonly found in stands of young woods, perturbed habitats, and on the borders of mature forests (Morano and Walker 1995), which provides alternative habitats for E. viteana outside vineyards. A sex pheromone-baited trap (Taschenberg et al. 1974, Taschenberg and Roelofs 1977) is typically hung from the vineyard trellis at 1.5 m to monitor activity of E. viteana, and is used by viticulturists to determine phenology of grape berry moth and to time control measures (Dennehy et al. 1990). Hoffman and Dennehy (1989) found that infestation by E. viteana was unpredictable from year to year, from vineyard to vineyard, and within vineyards, and Biever and Hostetter (1989) suggested this was because of variation in winter survival and/or the presence of wild grapes in surrounding woods, from which moths could immigrate into the vineyard. The presence of woods near the vineyard is a signiþcant factor in vineyard risk assessment because they harbor wild grape and are associated with greater vineyard infestations than at sites where no woods are found (Dennehy et al. 1990). However, woods containing Vitis spp. may also provide shelter and food sources for parasitoids of E. viteana (Seaman et al. 1990, Dennehy et al. 1990). By placing traps at the edge of the woods and in adjacent vineyards, Johnson et al. (1988) found that E. viteana emergence in woods is about a week earlier than at the edge of the vineyard. In addition to the differential timing of emergence, authors have implied that more E. viteana are at the edge of vineyards than inside vineyards because of damage assessments (Dennehy et al. 1990, Trimble 1993). This pattern suggests greater abundance of E. viteana in natural habitats than managed habitats (Hoffman and Dennehy 1989), as occurs with the redbanded leafroller, Argyrotaenia velutinana, in grapes (Biever and Hostetter 1989). Johnson et al. (1988) described early season abundance at the woods and vineyard edge, with a subsequent shift toward the center of the vineyard as the season progressed. This pattern was supported by Hoffman and Dennehy (1989), who trapped grape berry moths at 15 different positions along a transect from a vineyard, into woods, an alfalfa Þeld, another woods, and another vineyard. They showed that a higher percentage of moths were caught in the woods at the beginning of the season but near the time of harvest, more moths were caught inside the vineyard than anywhere else (Hoffman and Dennehy 1989). Similar patterns have been observed by Biever and Hostetter (1989) and Trimble et al. (1991). Height is an important consideration for understanding insect distribution and abundance, particularly when there is considerable difference in canopy height between habitats in which the insect is distributed (Derrick et al. 1992, Humphrey et al. 1999, Boiteau et al. 2000a). The woods and vineyard habitats of grape berry moth vary markedly in their structure and complexity. In vineyards, grapes are on trellises typically 2 m high, whereas in woods, they extend up to 25 m high, with wild grape plants climbing on mostly deciduous trees. Thus, a response to habitat structure will be an important component of this insectõs ecology in these two adjacent habitats. The relationship between vertical distribution of Lepidoptera and host distribution has been reported for a few species. Derrick et al. (1992) placed traps at two heights for monitoring European corn borer, Ostrinia nubilalis, in potatoes and corn, and found that traps placed in the crop canopy caught the highest number of moths. In apple orchards, captures of the oriental fruit moth, Cydia molesta, increased with trap height (Peterson 1926), and the greatest captures were obtained whenever traps were placed in the fruit zone, irrespective of height (Rothschild and Minks 1977). Riedl et al. (1979) and Howell et al. (1990) examined vertical variation in captures of codling moth Cydia pomonella, though these studies differ in their conclusions. Howell et al. (1990) did not Þnd a signiþcant variation in moth captures with height, but concluded the tree canopy had the greatest effect because captures depended on whether traps were hung inside the canopy or on its periphery. Riedl et al. (1979), however, found that maximum captures of C. pomonella were found at greater heights in the canopy. Studies of the effects of trap design and height on captures of the European vine moth (or European grape berry moth) Lobesia botrana, and the vine moth, Eupoecilia ambiguella led Gabel and Renczés (1985) to emphasize the importance of adapting sampling to the ethological and physiological characteristics of the particular pest. In Eastern North America, the grape berry moth exists in habitats of different structure, environmental conditions, and host distribution. The study described herein aimed to determine the relative distribution of this highly specialist herbivore in natural and cultivated habitats. The speciþc objectives of this study were to determine: (1) the vertical distribution of grape berry moth, (2) the horizontal distribution of grape berry moth across the vineyard-woods landscape, (3) the simultaneous vertical and horizontal distribution of grape berry moth through the season. Materials and Methods This study was conducted in juice grape (Vitis labrusca, var. Concord and Niagara) vineyards in Van Buren County, MI. All sites had a history of grape berry moth and were bordered on at least one side by deciduous woods. Relative moth abundance was measured using pheromone traps (large plasticdelta trap, Suterra LLC, Bend, OR) each baited with a lure containing 0.1 mg of syntheticsex pheromone of E. viteana (90:10 ratio of (Z)-9Ð12Acand (Z)-11Ð14Ac). Trap inserts were replaced as needed and pheromone lures were changed monthly, using the same batch of lures for all traps at each change. All traps were checked

3 October 2003 BOTERO-GARCÉS AND ISAACS: GRAPE BERRY MOTH DISTRIBUTION 1189 Fig. 1. Schematic representation (not to scale) of a study site in Pheromone traps (triangles) were hung at different heights on poles or ropes in Þve positions across the vineyard-woods habitats. Gray boxes represent the extent of the two habitats. weekly and the number of grape berry moth males recorded. Vertical Distribution. To determine variation in E. viteana abundance with trap height, two vertical transects of traps were placed 8.0Ð10.0 m apart on the edge of woods bordering four vineyards, in a complete block design. Traps were suspended by a loop of rope hung from a tree branch at least 10 m above the ground. Four pheromone traps were hung on each rope at 1.5, 3.0, 6.0, and 9.0 m above the ground. By using a rope at least 27 m long, the highest trap could be easily lowered, checked, and pulled back up. The number of male grape berry moths trapped was recorded weekly from 1 July to 21 October In 2000, grape berry moth vertical distribution was sampled next to the woods, on the grassy 7Ð14 m wide interface surrounding each vineyard, used by growers to maneuver machinery. Two 10 m tall PVC poles were placed at least 3 m from the woods edge at each of four vineyard-woods interfaces, in a complete block design. Each pole was constructed from PVC pipe, using a 3.3 m 10.4 cm i.d. piece connected to two 3.3 m 9.1 cm i.d. pieces that were joined by an overlapping 70 cm piece of 10.4 cm i.d. PVC. All pole connections were secured with steel bolts. A horizontal 2 m piece of PVC was attached to the top of the pole using a T-shaped PVC connector with a 3.3 cm eye-bolt at one end. This was used to hold the rope carrying pheromone traps, as described above. The base of each pole was buried 10 cm into the ground, and stabilized with four guy ropes attached 3 m below the top and tied to 1.2 m reinforced steel bars inserted into the ground. Traps were checked weekly from 3 June until 3 October Horizontal Distribution. To determine the relative abundance of grape berry moth in different parts of the vineyard-woods ecosystem, pheromone traps were placed 1.5 m above the ground (spaced 8.0Ð10 m apart) at four positions between the woods interior and vineyard interior, at six commercial vineyards bordered by deciduous woods. At each vineyard, a transect of traps was established at four positions from the woods interior to the vineyard interior. Three traps were placed 30 m inside the woods, Þve traps along the edge of those woods, Þve traps directly across the interface on the Þrst row of vines, and three traps 30 m inside the vineyard. Traps were checked weekly from 15 April to 21 October The average number of male E. viteana captured per trap was compared among the four positions for each of the three ßights to determine the temporal change in relative distribution between woods and vineyards. Vertical and Horizontal Distribution. During 2001, the vertical and horizontal distribution of E. viteana was simultaneously compared across the three ßights. This was done in two vineyards at each of four farms, at sites where vineyards were bordered by deciduous woods on at least one side. At each vineyard, 9.2 m tall steel telescoping poles (Channel Master, SmithÞeld, NC) were placed in each of four positions: at the edge of the woods, on the interface, at the edge of the vineyard and 30 m inside the vineyard, each with four pheromone traps hung at 1.5, 3.0, 6.0, and 9.0 m above the ground (Fig. 1). Inside the woods, where the poles could not be erected, loops of rope were hung from tree branches, at 1.5, 3.0, 6.0, 9.0 m. Wherever tree height allowed it, traps were also hung further up, at 12.2, and 15.2 m above the ground. Loops of rope were passed over tall tree branches using a bow with an adapted arrow and a string attached. Traps were installed during the spring, when few obstacles hindered the arrowõs path and total visibility of the canopy was possible. All traps were deployed by 19 April and checked weekly until 15 October Data Analysis. ShapiroÐWilkinson and KolmogorovÐSmirnov tests revealed that raw data were nonnormal, and so all were transformed (log n 1) to meet the criteria of normality and homogenous variance

4 1190 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 5 Table 1. Average number of Endopiza viteana caught at four different heights at the woods edge and the vineyard-woods interface in two different years Trap height (m) Mean SE moths caught per trap Woods edge (1999) Vineyard-woods interface (2000) c a c a b a a a Means within a column followed by the same letter are not significantly different (Tukey 0.05). among treatments. Main factors tested included height, position, and ßight. All analyses were performed with the SAS program (SAS Institute 1996). For all signiþcant factors, TukeyÕs test was performed to determine differences between means at the 5% probability level. In vertical distribution experiments, data were analyzed with a one-way analysis of variance (ANOVA) using PROC GLM (SAS, version 8.0). In the horizontal distribution experiment, data were analyzed with a one-way ANOVA using PROC MIXED (SAS, Version 8.0), with ßights as repeated measures. Data from the three-dimensional (vertical and horizontal and time) study were analyzed using an ANOVA with a two-way treatment structure (height and position) with repeated measures (ßights) using PROC MIXED (SAS, version 8.0). To test the significance of differences among positions only, data from the four heights were pooled within positions and analyzed for each ßight. Results Vertical Distribution. A total of 3,434 moths was trapped at the edge of the woods, and moth captures varied signiþcantly with height (F 3, , P ) (Table 1). Traps at 9.0 m caught signiþcantly more moths than traps at lower heights (P ), with 61% of all moths caught at 9.0 m. This compared with only 9.8% caught at the typical trap deployment height of 1.5 m. There was no signiþcant difference in captures between traps at 1.5 and 3.0 m (P 0.74). When traps were placed at the vineyard-woods interface moth captures were low (556 males) and did not vary signiþcantly with height (F 3, , P 0.15) Table 2. Average number of E. viteana caught per flight in traps placed at a height of 1.5 m in four different positions within the habitats sampled during 2000 Mean SE moths caught per trap Flight Woods Vineyard Inside Edge Edge Inside a ab b b a a a a b ab ab a Means within a row followed by the same letter are not signiþcantly different (Tukey 0.05). Fig. 2. Average number of male E. viteana caught per trap during each ßight in 2001, trapped at four heights across Þve positions in the vineyard-woods agroecosystem. (Table 1). The variability in these data reßects differences in populations among the four farms. Horizontal Distribution. The number of male moths captured varied according to the position of the traps in the vineyard-woods system and time of season. Almost three times as many moths (23,275) were caught in the woods habitat than in the vineyard habitat (8,453). During Flight 1, 84% of moths were caught in the woods, whereas 52% and 49% were trapped in the woods in ßights two and three, respectively, indicating variation in distribution between habitats over time. There were 12,058 moths (38% of the moths trapped all season) caught in Farm 2, and contrary to the trend observed in the other Þve farms, consistently fewer moths were trapped inside the vineyard during all three ßights at this farm. Analysis that included Farm 2 showed similar trends in abundance among positions to analysis excluding it, but because of the numerical difference between Farm 2 and the other Þve farms, the normality assumption

5 October 2003 BOTERO-GARCÉS AND ISAACS: GRAPE BERRY MOTH DISTRIBUTION 1191 Table Average number of E. viteana caught in traps per position ( m heights pooled), during three flights sampled during Mean SE moths caught per trap Flight Woods Vineyard Interface Inside Edge Edge Inside a b b b b a b b b a ab ab b b a Means within a row followed by the same letter are not signiþcantly different (Tukey 0.05). could not be met. Therefore, Farm 2 was excluded from further analysis. In the Þve remaining farms, total moth captures were signiþcantly different among the three ßights of 2000 (F 2, , P ) and there was a signiþcant interaction between positions and ßights (F 6, , P ) (Table 2). During Flight 1, 71.5% of moths were caught in the woods habitat, a proportion that decreased to 46.8% during Flight 2, and to 27.4% in Flight 3. Although the difference in relative abundance of grape berry moth was not signiþcant among vineyard positions, more moths were captured inside the vineyard than at the vineyard edge for Flights 2 and 3 (Table 2). Vertical and Horizontal Distribution. Captures of grape berry moth varied signiþcantly across habitats (positions) (F 4, , P ) and during each individual ßight (F 2, , P ) (Fig. 2), with a signiþcant position by ßight interaction (F 38, , P ). Combining captures of E. viteana between 1.5 and 9.0 m, a 1.9-fold decrease in moth capture from Flight 1 (total of 2,994 moths) to Flight 2 (1,561) and a subsequent 2.6-fold decrease to Flight 3 (603) were observed (Table 3). During Flight 1, 86% of the moths were caught in the woods habitat (both inside and edge) compared with only 10% caught in the vineyard habitat (both edge and inside). However, during Flight 2, the proportion of moths trapped in the woods habitat decreased to 57% and increased in the vineyard habitat to 40%. Captures were similar in both habitats during Flight 3, with 45% of captures in the woods and 49% in the vineyards. Simultaneous sampling of E. viteana adults across horizontal and vertical gradients conþrmed the pattern observed in separate studies of horizontal and vertical distribution in Captures in the interface were low throughout the season (Fig. 2), and more moths were trapped inside the vineyard that at the edges. This difference was signiþcant in Flights 2 and 3 (Table 3). When relative abundance was compared across heights, some clear patterns were seen (Fig. 2). Moth captures varied signiþcantly according to height (F 3, , P ), and this variation was signiþcantly inßuenced by ßight and position (F 38, , P ). The capture of moths at different heights depended on where (position and habitat) the trap was placed (at 1.5 m F 4, , at 3.0 m F 4, , at 6.0 m F 4, , at 9.0 m F 4, ; P ). At all positions except the interface (F 3, , P 0.19), there was a signiþcant variation in moth relative abundance among heights (inside woods F 3, , at the woods edge F 3, , at the vineyard edge F 3, , and inside the vineyard F 3, ; P ), with the greatest number of moths caught in the higher traps in the woods habitat and in the lowest traps in the vineyard habitat (Fig. 2). When captures at 1.5 m were considered separately because of their relevance to monitoring for this insect, more moths were always captured inside the vineyard than inside the woods (Fig. 2), though this Fig. 3. Average number of male E. viteana per trap during each ßight, trapped at six heights inside woods adjacent to vineyards during Within each ßight, bars with the same letters are not signiþcantly different (Tukey 0.05).

6 1192 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 5 difference was not signiþcant during the Þrst ßight. At the edge and interior of the vineyard, signiþcantly more moths were trapped at 1.5 m than at any other height (Tukey P between 1.5 and 6.0 m, P between 1.5 and 9.0 m at the vineyard edge, and P for the same comparisons inside the vineyard), with very few moths found in traps placed above the canopy (Fig. 2). When the full height of the tree canopy in wild habitats was taken into consideration, the greatest captures of moths were made in traps at 12.2 and m height. Indeed, moth captures increased signiþcantly with height of trap inside the woods (F 5, , P ), so that 76.1% of moths captured in the vertical transects within the woods were caught at or above 9.0 m (Fig. 3). This change in relative abundance with height in the woods was consistent across ßights (Fig. 3), and the change among ßights was consistent with results during 2000 (Table 2). Discussion Our results indicate there is differential spatial and temporal distribution of grape berry moth across vineyard-woods landscapes. Relative abundance of grape berry moth was found to vary signiþcantly with the type of habitat in which this insect was sampled, and with the height at which samples were taken. The greatest captures of E. viteana males were made during Flight 1, with decreasing captures for successive ßights. There are several possible explanations for this pattern. Hamstead et al. (1972) found a similar pattern in A. velutinana, and suggested that early in the season lower temperatures favored traps over sexually mature females, whose release of pheromone was reduced. Another explanation could be that diapause frequency in E. viteana increases after 25 June (Flight two and three) as daylength shortens (Nagarkatti et al. 2001). Tobin et al. (2002) suggested that E. viteana is protandrous, which would explain abundant captures of males early in the season when only the lures inside traps are releasing pheromone. The decreasing captures of males in successive ßights have been explained by increasing abundance of virgin female moths, which increasingly compete with the pheromone traps as the population grows through the season (Howell 1974, Hoffman and Dennehy 1989, Dennehy et al. 1990, Aslam et al. 1990). Sampling across vineyard-woods habitats throughout the season showed that captures of E. viteana vary signiþcantly with sampling position and trap height, a trend that could be because of the response of this species to the structure and composition of its habitat. Although results obtained from traps at 1.5 m agree with previous Þndings (Hoffman and Dennehy 1989, Lewis and Johnson 1999), by placing traps between 1.5 and 9.0 m above the ground in these different habitats, we have shown that a majority (90.2% in 1999) of E. viteana males in woods are consistently distributed above the typical height for trap placement (Table 1; Figs. 2 and 3). Hoffman and Dennehy (1989) found that pheromone traps placed at wood edges captured few moths even though high numbers of eggs were deposited in the same area on wild grapes, suggesting that male E. viteana emigrate from areas of oviposition activity. The number of times female E. viteana mate is not known, but if they usually mate only once as found for L. botrana (Torres-Vila et al. 1997), emigration from areas of oviposition would improve a male mothõs chance of locating virgin females. However, in view of our results, previous studies using traps within easy reach have probably missed moths ßying high in the woods. Traps placed at different heights in the woods canopy showed that more moths were captured high in the woods than in traps placed at 1.5 m in the vineyard. This suggests that, rather than a shift in abundance of this species from the woods to the vineyard as the season progresses, there is a distribution of moths in which their abundance is greatest in the higher canopy. Relative abundance is highest in the woods throughout the season, but because of the typical 1.5 m monitoring position used, this has remained unnoticed. Low captures of E. viteana in traps placed in the vineyard-woods interface in 2000 and 2001, coupled with the similar captures at different heights (Table 1; Fig. 2.) indicate that the lack of host plant in this position provided no host substrate to which the moths could respond. In vineyards, the greatest moth captures were consistently within the canopy, with few moths captured above 1.5 m. Taken together with the results in woods described above, these results agree strongly with those of Hoffman and Dennehy (1989), suggesting that E. viteana distribution is tightly coupled to the structure of the habitat where its host is present. Wild grapes comprise four species of Vitis in the Eastern United States and are common throughout wild and perturbed habitats (Morano and Walker 1995). At the edge of woods, vines grow on border trees, sometimes covering them from the ground to the canopy top. Inside the woods, they grow on trees, developing fully into the canopy where light intensity is greatest. The majority of fruiting occurs at this height, typically 16Ð18 m high in the deciduous woods surrounding Michigan vineyards (N.B.-G., unpublished data). The variation in captures of male moths with height may be a response to canopy height, fruit distribution, or virgin female distribution. Correlations between fruit moth abundance and canopy height have been described before for the two grape pests E. ambiguella and L. botrana (Gabel and Renczés 1985), for C. pomonella (Riedl et al. 1979, Howell et al. 1990) and for C. molesta (Rothschild and Minks 1977). Vertical distribution of foraging insects can be tightly linked to resource vertical distribution (Muirhead- Thompson 1991, Cisneros and Rosenheim 1998) and there can be species-speciþc (Nyrop and Simmons 1986) and family-speciþc (Taylor 1974, Humphrey et al. 1999, Boiteau et al. 2000a, Boiteau et al. 2000b) vertical distribution patterns driven by dispersal, foraging, mating and oviposition behaviors. There is an adaptive beneþt to behaviors that maximize abundance of male E. viteana in regions where

7 October 2003 BOTERO-GARCÉS AND ISAACS: GRAPE BERRY MOTH DISTRIBUTION 1193 grape clusters are numerous, because female oviposition is strictly on this resource (Clark and Dennehy 1988). Vertical distribution of eggs within the vineyard canopy is closely correlated with fruit density (Clark and Dennehy 1988) and so mated female E. viteana are assumed to be most abundant near their oviposition substrate, as predicted for specialized herbivores (Miller and Strickler 1984, Hamilton and Zalucki 1993). It is not known whether virgin female E. viteana release pheromone only when on grape clusters but the likelihood of males Þnding females is assumed to be greatest if they are in proximity to this oviposition site. Male C. pomonella are trapped in much greater numbers in pheromone traps placed in the host canopy compared with those placed outside the canopy (Howell et al. 1990), and Riedl et al. (1979) argued that more C. pomonella males were caught in traps placed in the higher tree canopy because of the preference for mating near the canopy top. In another polyphagous insect, the tortricid Archips podana, morphological and temporal heterogeneity of populations is tightly related to larval food preference (Safonkin 1988). Evidence for larval habitat directly inßuencing mating behavior of adult moths has recently been described by Takacs et al. (2002) with webbing clothes moths. In this case, males seek larval habitats and produce pheromone and sonic signals to enhance recruitment of females to a patchy and temporary resource. Our vertical sampling results complement the study by Hoffman and Dennehy (1989) by showing that moths remain abundant high in the woods canopy throughout the season. These Þndings can help answer questions posed by these and other researchers (Dennehy et al. 1990, Trimble 1993, Lewis and Johnson 1999) of why few male E. viteana are trapped in woods adjacent to vineyards with high levels of cluster infestation and why pheromone disruption is less effective at vineyard borders (Taschenberg et al. 1974, Trimble et al. 1991, Karg and Sauer 1995). Explanations of high larval infestations where few male moths have been caught have centered on mated females ßying into the vineyard to lay eggs, both in E. viteana (Taschenberg et al. 1974, Biever and Hostetter 1989, Trimble et al. 1991) and in L. botrana (Karg and Sauer 1995). Our Þndings show that a large proportion of the adult population of E. viteana is in areas outside those targeted by management programs, reinforcing the need to consider the whole landscape when studying the ecology of native insects (Burel et al. 2000) and tortricids in particular (Barrett 2000). This approach will also be of value when considering enhancement of biological control (Wratten and Thomas 1990, Marino and Landis 2000), or cultural practices such as removal of wild hosts to reduce the impact of grape berry moth on grape production. Movement of insects between wild and cultivated habitats has been reviewed by Macdonald and Smith (1990), Woiwod and Stewart (1990), and Ekbom (2000). Schumacher et al. (1997)) stated that both mated and virgin female C. pomonella are capable of movement between orchards, with important implications for pest management strategies such as pheromone disruption and resistance management (Dorn et al. 1999). Trimble (1993) concluded that high levels of larval infestation by E. viteana at vineyard borders could be a result of mated females entering the vineyard from woods to lay eggs, but direct movement of E. viteana has as yet to be conclusively demonstrated. Discovery of a female attractant, as recently described for C. pomonella (Light et al. 2001), would greatly assist in determining the signiþcance of immigration by mated female moths from wild grape into adjacent vineyards. Acknowledgments We thank Keith Mason, ZsoÞa Szendrei, Rodrigo Mercader, Nikhil Mallampalli, Katie Hohauser, Kelly Bahns, Jeff Eastman, Darek Gajek, Sergey Balyinski, Doug Murray, Peter McGhee, Gary Parsons, and Deborah McCullough for their assistance with this research. We would like to acknowledge the advice received from the Michigan State University Statistical Consulting Center, particularly from Corina Sirbu. We particularly thank the following grape growers for access to their land: Rick Brown, Louie Bonamego, Ed Oxley, Bill Mihelich, Don Thornton, and John Mann. Funding for this research was made available by National Grape Cooperative, Michigan State Horticultural Society, Michigan Grape and Wine Council, Project GREEEN, and the Michigan Agricultural Experiment Station. We are also grateful for the use of the Trevor Nichols Research Complex facilities. This study was conducted in partial fulþllment of a Ph.D. by Natalia Botero-Garcés. References Cited Aslam, M., G. E. Wilde, and T. L. Harvey Monitoring ßight activity of sunßower moth (Lepidoptera: Pyralidae) in Kansas. Environ. Entomol. 19: 1639Ð1645. Barrett, G. W The impact of corridors on arthropod populations within simulated agrolandscapes, pp. 71Ð84. In B. Ekbom, M. E. Irwin, and Y. Robert [eds.], Interchanges of insects between agricultural and surrounding landscapes. Kluwer Academic Publishers, Dordrecht, The Netherlands. Biever, K. D., and D. L. Hostetter Phenology and pheromone trap monitoring of the grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae) in Missouri. J. Entomol. Sci. 24: 472Ð481. Boiteau, G., W.P.L. Osborn, X. Xiong, and Y. Bousquet. 2000a. The stability of vertical distribution proþles of insects in air layers near the ground. Can. J. Zool. 78: 2167Ð2173. Boiteau, G., Y. Bousquets, and W. Osborn. 2000b. Vertical and temporal distribution of Carabidae and Elateridae in ßight above an agricultural landscape. Environ. Entomol. 29: 1157Ð1163. Burel, F., J. Baudry, Y. Delettre, S. Petit, and N. Morvan Relating insect movements to farming systems in dynamiclandscapes, pp. 5Ð32. In B. Ekbom, M. E. Irwin, and Y. Robert [eds.], Interchanges of insects between agricultural and surrounding landscapes. Kluwer AcademicPublishers, Dordrecht, The Netherlands. Cisneros, J. J., and J. A. Rosenheim Changes in the foraging behavior, within-plant vertical distribution, and microhabitat selection of a generalist insect predator: an age analysis. Environ. Entomol. 27: 949Ð957.

8 1194 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 5 Clark, L. G., and T. J. Dennehy Oviposition behavior of grape berry moth. Entomol. Exp. Appl. 47: 223Ð230. Dennehy, T. J., C. J. Hoffman, J. P. Nyrop, and M. C. Saunders Development of low-spray, biological and pheromone approaches for control of grape berry moth, Endopiza viteana Clemens, in the Eastern United States, pp. 261Ð282. In N. Bostanian, L. Wilson, and T. J. Dennehy [eds.], Monitoring and integrated management of arthropod pests of small fruit crops. Intercept Ltd., Andover, England. Derrick, M. E., J. W. van Duyn, C. E. Sorenson, and G. G. Kennedy Effect of pheromone trap placement on capture of male European corn borer (Lepidoptera: Pyralidae) in three North Carolina crops. Environ. Entomol. 21: 240Ð246. Dorn, S., P. Schumacher, C. Abivardi, and R. Meyhofer Global and regional pest insects and their antagonists in orchards: spatial dynamics. Agric. Ecosyt. Environ. 73: 111Ð118. Dozier, H. L., L. L. Williams, and H. G. Butler Life history of the grape berry moth in Delaware. University of Delaware Agricultural Experimental Station Bull Ekbom, B Interchanges of insects between agricultural and surrounding landscapes, pp. 1Ð3. In B. Ekbom, M. E. Irwin, and Y. Robert [eds.], Interchanges of insects between agricultural and surrounding landscapes. Kluwer Academic Publishers, Dordrecht, The Netherlands. Gabel, B., and V. Renczés Factors affecting the monitoring of ßight activity of Lobesia botrana and Eupoecilia ambiguella (Lepidoptera, Tortricidae) by pheromone traps. Acta Entomol. Bohemos. 82: 269Ð277. Hamilton, J. G., and M. P. Zalucki Interactions between a specialist herbivore, Crocidosema plebejana, and its host plants Malva parviflora and cotton, Gossypium hirsutum: oviposition preference. Entomol. Exp. Appl. 66: 207Ð212. Hamstead, E. O., R. E. Dolphin, and W. Roelofs Field test of virgin female and syntheticsex-lure traps for male redbanded leafrollers. Environ. Entomol. 1: 488Ð489. Hoffman, C. J., and T. J. Dennehy Phenology, movement, and within-þeld distribution of the grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae), in New York vineyards. Can. Entomol. 121: 325Ð335. Hoffman, C. J., T. J. Dennehy, and J. P. Nyrop Phenology, monitoring, and control decision components of the grape berry moth (Lepidoptera: Tortricidae) risk assessment program in New York. J. Econ. Entomol. 85: 2218Ð2227. Howell, J. F The competitive effect of Þeld populations of codling moth on sex attractant trap efþciency. Environ. Entomol. 3: 803Ð807. Howell, J. F., R. S. Schmidt, D. R. Horton, S.U.K. Khattak, and L. D. White Codling moth: male moth activity in response to pheromone lures and pheromone-baited traps at different elevations within and between trees. Environ. Entomol. 19: 573Ð577. Humphrey, J. W., C. Hawes, A. J. Peace, R. Ferris-Kaan, and M. R. Jukes Relationships between insect diversity and habitat characteristics in plantation forests. For. Ecol. 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Walker Soils and plant communities associated with three Vitis species. Am. Midl. Nat. 134: 254Ð263. Muirhead-Thomson, R. C Trap responses of ßying insects: the inßuence of trap design on capture efþciency. Academic Limited, London, England. Nagarkatti, S., P. C. Tobin, and M. C. Saunders Diapause induction in the grape berry moth (Lepidoptera: Tortricidae). Environ. Entomol. 30: 540Ð544. Nyrop, J. P., and G. A. Simmons Temporal and spatial activity patterns of an adult parasitoid, Glypta fumiferanae (Hymenoptera: Ichneumonidae), and their inßuence on parasitism. Environ. Entomol. 15: 481Ð487. Peterson, A Additional information on baits attractive to the oriental peach moth, Laspeyresia molesta Busck, J. Econ. Entomol. 19: 429Ð439. Pettit, R. H The grape berry moth in (MAES) Michigan Agricultural Experimental Station Quarterly Bull. vol. 14, 4 pp. East Lansing, MI. Riedl, H., S. A. Hoying, W. W. Barnett, and J. E. DeTar Relationship of within-tree placement of the pheromone trap to codling moth catches. Environ. Entomol. 8: 765Ð 769. Rothschild, G.H.L., and A. K. Minks Some factors inßuencing the performance of pheromone traps for oriental fruit moth in Australia. Entomol. Exp. Appl. 22: 171Ð182. Safonkin, A. F Infrastructure of the population of the great brown tortricid Archips podana Sc. (Lepidoptera: Tortricidae) in relation to coincidence with its various food-plants. Dokl. Akad. Nauk. SSSR. 296: 499Ð500. SAS Institute PROC userõs manual, version 8.0, 5 th ed. SAS Institute, Cary, NC. Schumacher, P., A. Weyeneth, D. C. Weber, and S. Dorn Long ßights in Cydia pomonella L. (Lepidoptera:

9 October 2003 BOTERO-GARCÉS AND ISAACS: GRAPE BERRY MOTH DISTRIBUTION 1195 Tortricidae) measured by a ßight mill: inßuence of sex, mated status and age. Physiol. Entomol. 22: 149Ð160. Seaman, A. J., J. P. Nyrop, and T. J. Dennehy Egg and larval parasitism of the grape berry moth (Lepidoptera: Tortricidae) in three grape habitats in New York. Environ. Entomol. 19: 764Ð770. Slingerland, M. V The grape berry moth. Cornell University Agricultural Experimental Station of the College of Agriculture Bull. 223: 43Ð60. Takács, S., G. Gries, and R. Gries Where to Þnd a mate? Resource-based sexual communication of webbing clothes moth. Naturwiss 89: 57Ð59. Taschenberg, E. F., R. T. Cardé, and W. L. Roelofs Sex pheromone mass trapping and mating disruption for control of redbanded leaf roller and grape berry moths in vineyards. Environ. Entomol. 3: 239Ð242. Taschenberg, E. F., and W. L. Roelofs Mating disruption of the grape berry moth, Paralobesia viteana, with pheromone released from hollow Þbers. Environ. Entomol. 6: 761Ð763. Taylor, L. R Insect migration, ßight periodicity and the boundary layer. J. Anim. Ecol. 43: 225Ð238. Tobin, P. C., S. Nagarkatti, and M. C. Saunders Diapause maintenance and termination in the grape berry moth (Lepidoptera: Tortricidae). Environ. Entomol. 31: 708Ð713. Torres-Vila, L. M., J. Stockel, and M. C. Rodríguez-Molina Physiological factors regulating polyandry in Lobesia botrana (Lepidoptera: Tortricidae). Physiol. Entomol. 22: 387Ð393. Trimble, R., D. Pree, P. Vickers, and K. W. Ker Potential of mating disruption using sex pheromone for controlling the grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae), in Niagara peninsula, Ontario vineyards. Can. Entomol. 123: 451Ð460. Trimble, R EfÞcacy of mating disruption for controlling the grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae), a case study over three consecutive growing seasons. Can. Entomol. 125: 1Ð9. Woiwod, I. P., and J. A. Stewart Butterßies and mothsñmigration in the agricultural habitat, pp. 189Ð202. In R.G.H. Bunce and D. C. Howard [eds.], Species dispersal in agricultural habitats. Belhaven Press, London, England. Wratten, S. D., and C.F.G. Thomas Farm-scale spatial dynamics of predators and parasitoids in agricultural landscapes, pp. 219Ð237. In R.G.H. Bunce and D. C. Howard [eds.], Species dispersal in agricultural habitats. Belhaven Press, London, England. Received for publication 31 January 2003; accepted 7 July 2003.

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